Boggs, C. L. | Search bioRxiv

bioRxiv2024

Genetic Mechanisms underlying Preference-Performance Mismatches: Insights from a Specialized Native Herbivore on an Invasive Toxic Plant

Specialist phytophagous insects have a narrow hostplant range for optimal development and survival. Mismatches between female oviposition preference and larval performance can lead to high fitness costs. Understanding the mechanistic basis of this decoupling can help us understand evolutionary constraints and aid in predicting outcomes of error-prone oviposition. We investigated the causes for preference-performance mismatches in a specialist native herbivore laying eggs on an invasive toxic plant. Transcriptomic analyses revealed no differential gene expression in gustatory/olfactory organs of adult females with different oviposition preference, but larvae exhibit host-plant-specific gene expression signatures. The larvae feeding on toxic plants showed lower expression of specialized detoxification enzymes and higher expression of general digestive enzymes, indicating the inability of larvae to detoxify toxic compounds present in the toxic plants. We additionally found that genes related to successful detoxification and adaptive feeding were enriched in larvae feeding on native plants, while genes related to toxic responses, apoptosis and accelerated development were enriched in larvae feeding on toxic plants. Our findings dissect genetic mechanisms behind preference-performance mismatches, quantifying the impact of error-prone oviposition on larval performance in specialized species interaction.

evolutionary biology↗

bioRxiv2023

Gene family evolution in brassicaceous-feeding insects: Implications for adaptation and host plant range.

Herbivores have a defined range of hostplants that they can feed on, which is mediated by underlying detoxification and sensory repertoires. Insects that feed on Brassicaceae represent one of the striking examples of co-evolutionary arms race. Insects specialized on Brassicaceae have evolved specific mechanisms to detoxify mustard oils (glucosinolates), while generalist species use detoxification enzymes that act on a variety of substrates. Understanding the gene evolution of detoxification and sensory repertoire in specialist and generalist Brassicaceae feeders will shed light on the processes involved in mediating hostplant ranges in herbivores. We use a comparative phylogenomic approach in 12 lepidopterans that feed on Brassicaceae, ranging from specialist to pests in their host range to examine the gene family expansion of detoxification and sensory gene families. We found that gene family expansions and contractions were larger in generalist herbivores compared to specialist herbivores. Gene evolutionary rate of detoxification genes reflected hostplant range where generalists had a higher evolutionary rate of detoxification genes that act on wide substrates while specialists had a higher evolutionary rate in genes that conjugate toxic compounds to hydrophilic byproducts. Our analysis on the nitrile specifier gene, a key innovation for feeding on Brassicaceae, indicated pervasive purifying selection with lineage specific differences in selection. Our results add to the growing body of work addressing gene family evolution and its role in hostplant range and specialization in insects.

evolutionary biology↗